Abstract
Global climate change is altering thermal cycles in soils during late winter, a transition that may directly threaten seed survival via abiotic stress, facilitate infection by soil-borne pathogens, or both. Using field-collected soil and seeds of the perennial bunchgrass Elymus canadensis, we tested the hypothesis that soil freeze–thaw events limit survival within the soil through direct effects on seed persistence and amplification of soil pathogen attack using a factorial experiment that manipulated freeze–thaw cycles (constant freeze vs. freeze–thaw) and fungicide addition. Freeze–thaw treatment resulted in lower seedling emergence and delayed emergence time relative to constant-freeze controls. Fungicide-treated soils had greater emergence relative to untreated soils; the lowest seedling emergence was observed in no-fungicide, freeze–thaw-treated soils (<1 %). The strong effects of thermal variability and fungi on seeds were mitigated through interactions at the seed–soil interface, as subsequent experiments showed that fungicide and freeze–thaw treatments alone do not influence dormancy. Our work demonstrates that changes in freeze–thaw events directly limit seedling emergence, delay seedling phenology, and provide opportunities for fungal pathogens to limit seed persistence. As recruitment from seeds is a key determinant of plant population dynamics, these results suggest that climatic variation may generate unique consequences for populations under changing climate regimes.
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References
Agrios GN (1997) Plant pathology, 4th edn. Academic, San Diego
Baskin CC, Baskin JM (1998) Seeds: ecology, biogeography, evolution of dormancy and germination. Academic, New York
Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1–7. http://CRAN.R-project.org/package=lme4. Accessed 30 June 2014
Beckstead J, Meyer SE, Connolly BM, Huck MB, Street LE (2010) Cheatgrass facilitates spillover of a seed bank pathogen onto native grass species. J Ecol 98:168–177
Bell KL, Amen RD (1970) Seed dormancy in Luzula spicata and L. parviflora. Ecology 51:492–496
Bigler C, Bräker OU, Bugmann H, Dobbertin M, Rigling A (2006) Drought as an inciting mortality factor in scots pine stands of the Valais, Switzerland. Ecosystems 9:330–343
Blaney CS, Kotanen PM (2001) Effects of fungal pathogens on seeds of native and exotic plants: a test using congeneric pairs. J Appl Ecol 38:1104–1113
Brudvig LA, Damschen EI (2011) Land-use history, historical connectivity, and land management interact to determine longleaf pine woodland understory richness and composition. Ecography 34:257–266
Cannell MGR, Smith RI (1986) Climatic warming, spring budburst, and forest damage on trees. J Appl Ecol 23:177–191
Cleavitt NL, Fahey TJ, Groffman PM, Hardy JP, Henry KS, Driscoll CT (2008) Effects of soil freezing on fine roots in a northern hardwood forest. Can J For Res 38:82–91
Coakley SM, Scherm H, Chakraborty S (1999) Climate change and plant disease management. Annu Rev Phytopathol 37:399–426
Cook RJ, Papendick RI (1972) Influence of water potential of soils and plants on root disease. Annu Rev Phytopathol 10:349–374
Crist TO, Friese CF (1993) The impact of fungi on soil seeds: implications for plants and granivores in a semiarid shrub-steppe. Ecology 74:2231–2239
Dalling JW, Davis AS, Schutte BJ, Arnold AE (2011) Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community. J Ecol 99:89–95
Dyer JL, Mote TL (2006) Spatial variability and trends in observed snow depth over North America. Geophys Res Lett 33:1–6
Dyer AR, Fenech A, Rice KJ (2000) Accelerated seedling emergence in interspecific competitive neighbourhoods. Ecol Lett 3:523–529
Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modeling, and impacts. Science 289:2068–2074
Egli T, Goto M, Schmidt D (1975) Bacterial wilt, a new forage grass disease. Phytopathol Z 82:111–121
Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand Oaks. http://socserv.socsci.mcmaster.ca/jfox/Books/Companion
Geiger R (1965) The climate near the ground. Harvard University Press, Cambridge
Gu L, Hanson PJ, Post WM, Kaiser DP, Yang B, Nemani R, Pallardy SG, Meyers T (2008) The 2007 eastern US spring freeze: increased cold damage in a warming world? Bioscience 58:253–262
Hampe A (2011) Plants on the move: the role of seed dispersal and initial population establishment for climate-driven range expansions. Acta Oecologia 37:666–673
Harrison XA (2014) Using observation-level random effects to model overdispersion in count data in ecology and evolution. PeerJ 2:e616. doi:10.7717/peerj.616
Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162
Henry HAL (2007) Soil freeze–thaw cycle experiments: trends, methodological weaknesses and suggested improvements. Soil Biol Biochem 39:977–986
Henry HAL (2008) Climate change and soil freezing dynamics: historical trends and projected changes. Clim Change 87:421–434
Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362
Jactel H, Petit J, Desprez-Loustau M-L, Delzon S, Piou D, Battisti A, Koricheva J (2012) Drought effects on damage by forest insects and pathogens: a meta-analysis. Glob Change Biol 18:267–276
Kirkpatrick BL, Bazzaz FA (1979) Influence of certain fungi on seed germination and seedling survival of four colonizing annuals. J Appl Ecol 16:515–527
Kreyling J (2010) Winter climate change: a critical factor for temperate vegetation performance. Ecology 91:1939–1948
Kreyling J, Haei M, Laudon H (2012a) Absence of snow cover reduces understory plant cover and alters plant community composition in boreal forests. Oecologia 168:577–587
Kreyling J, Peršoh D, Werner S, Benzenberg M, Wöllecke J (2012b) Short-term impacts of soil freeze-thaw cycles on roots and root-associated fungi of Holcus lanatus and Calluna vulgaris. Plant Soil 353:19–31
Leishman MR, Masters GJ, Clarke IP, Brown VK (2000) Seed bank dynamics: the role of fungal pathogens and climate change. Funct Ecol 14:293–299
Lenth RV, Hervé M (2014) lsmeans: least-squares means. R package version 2.13. http://CRAN.R-project.org/package=lsmeans. Accessed 30 June 2014
Malmstrom CM, McCullough AJ, Johnson HA, Newton LA, Borer ET (2005) Annual grasses indirectly increase virus incidence in California native perennial bunchgrasses. Oecologia 145:153–164
Mayr S, Gruber A, Bauer H (2003) Repeated freeze–thaw cycles induce embolism in drought stressed conifers (Norway spruce, stone pine). Planta 217:436–441
Meyer SE, Merrill KT, Allen PS, Beckstead J, Norte AS (2014) Indirect effects of an invasive annual grass on seed fates of two native perennial grass species. Oecologia 174:1401–1413
Mitschunas N, Filser J, Wagner M (2009) On the use of fungicides in ecological seed burial studies. Seed Sci Res 19:51–60
Mordecai EA (2013) Despite spillover, a shared pathogen promotes native plant persistence in a cheatgrass-invaded grassland. Ecology 94:2744–2753
Olff H, Hoorens B, de Goede RGM, van der Putten WH, Gleichman JM (2000) Small-scale shifting mosaics of two dominant grassland species: the possible role of soil-borne pathogens. Oecologia 125:45–54
Orrock JL, Christopher CC (2010) Density of intraspecific competitors determines the occurrence and benefits of accelerated germination. Am J Bot 97:694–699
Pauli JN, Zuckerberg B, Whiteman JP, Porter WW (2013) The subnivium: a deteriorating seasonal refugium. Front Ecol Environ 11:260–267
R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
Regehr DL, Bazzaz FA (1979) The population dynamics of Erigeron canadensis, a successional winter annual. J Ecol 67:923–933
Ross MA, Harper JL (1972) Occupation of biological space during seedling establishment. J Ecol 60:77–88
Scherm H (2004) Climate change: can we predict the impacts on plant pathology and pest management? Can J Plant Pathol 26:267–273
Seabloom EW, Harpole WS, Reichman OJ, Tilman D (2003) Invasion, competitive dominance, and resource use by exotic and native California grassland species. Proc Natl Acad Sci USA 100:13384–13389
Sharma S, Szele Z, Schilling R, Munch JC, Schloter M (2006) Influence of freeze–thaw stress on the structure and function of microbial communities and denitrifying populations in soil. Appl Environ Microbiol 72:2148–2154
Sinha T, Cherkauer KA (2010) Impacts of future climate change on soil frost in the midwestern United States. J Geophys Res 115:1–16
Stanghellini ME, Hancock JG (1971a) The sporangium of Pythium ultimum as a survival structure in soil. Phytopathology 61:157–164
Stanghellini ME, Hancock JG (1971b) Radial extent of the bean spermosphere and its relation to the behavior of Pythium ultimum. Phytopathology 61:165–168
Therneau T (2014) A package for survival analysis in S. R package version 2.37–7. http://CRAN.R-project.org/package=survival
Thompson K, Grime JP (1979) Seasonal variation in the seed banks of herbaceous species in ten contrasting habitats. J Ecol 67:893–921
Tilman D (1997) Community invasibility, recruitment limitation, and grassland biodiversity. Ecology 78:81–92
Turnbull LA, Crawley MJ, Rees M (2000) Are plant populations seed-limited? A review of seed sowing experiments. Oikos 88:225–238
Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363
Verdú M, Traveset A (2005) Early emergence enhances plant fitness: a phylogenetically controlled meta-analysis. Ecology 86:1385–1394
Vyas SC (1988) Nontarget effects of agricultural fungicides. CRC, Boca Raton
Walck JL, Hidayati SN, Dixon KW, Thompson KEN, Poschlod P (2011) Climate change and plant regeneration from seed. Glob Change Biol 17:2145–2161
Acknowledgments
We thank Cathie Bruner and the Lakeshore Nature Preserve for permitting access to field plots. We thank the Orrock Lab, Dr. John Dwyer, and two anonymous reviewers for helpful comments on an earlier draft of this manuscript. These experiments comply with the current laws of the United States of America. This work was funded by the UW Vilas Associates Program, Guyer Fund postdoctoral research support, and AFRI-NIFA Fellowship grant #2014-02074 awarded to J.L. Orrock and B.M. Connolly.
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The authors declare that they have no conflict of interest.
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Communicated by John Dwyer.
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Connolly, B.M., Orrock, J.L. Climatic variation and seed persistence: freeze–thaw cycles lower survival via the joint action of abiotic stress and fungal pathogens. Oecologia 179, 609–616 (2015). https://doi.org/10.1007/s00442-015-3369-4
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DOI: https://doi.org/10.1007/s00442-015-3369-4